Aspects of Reproduction and Development in the Prairie Vole (Microtus ochrogaster).

by Henry S. Fitch.

INTRODUCTION

The prairie vole is by far the most abundant mammal on the University of Kansas Natural History Reservation and on gra.s.sland areas throughout northeastern Kansas. This vole therefore affects the vegetation, perhaps more than any other native vertebrate, and it is an important food source for most of the vertebrate predators.

Since the Reservation was established, in 1948, more data have been acc.u.mulated concerning this vole than for any other species of animal there. From February, 1950, to February, 1954, a grid of live-traps at 50-foot intervals was set for several days each month in a three-acre field inhabited by voles, and the population of marked individuals was studied throughout the four-year period. From November, 1953, to June, 1956, a half-acre trap grid with 20-foot interval was used on an area adjoining the three-acre field. Other trap lines in somewhat different habitats were maintained for shorter periods as a basis for comparison. By June, 1956, a total of some 3550 voles had been caught and recorded 14,750 times in all.

The present report is a preliminary attempt to a.n.a.lyze, in part, these extensive data, and is concerned with certain phases of the species' reproduction and growth that have bearing on the observed population changes from month to month and from year to year on the Reservation.

Through the studies of Jameson (1947) and Martin (1956), both made in the same general area as my own, and several earlier studies, the life history and ecology of the prairie vole are already well known.

The present report, with much larger amounts of data, further clarifies certain phases of the ecology; and by using types of data not available to Jameson and Martin I have dealt with some topics not included in their reports.

Previous studies of growth in _Microtus_ have been based almost entirely on weights. However, the weight of an individual vole may fluctuate widely over a short period, depending on pregnancy and parturition, length of time in a trap without food, availability of moisture, and other factors. In the course of my study, in 1954 and 1955, and parts of 1953 and 1956, measurements of total length, in addition to weights, were recorded for most of the voles live-trapped.

To test the accuracy of measurements, successive readings were compared in individual voles that were already of large adult size and that presumably either had stopped growing or were growing so slowly that the gain was scarcely detectable in the relatively short periods involved. For 200 such readings 33 per cent were just the same as previous records for the same animals, 24 per cent deviated by 1 mm., 22 per cent deviated by 2 mm., 15 per cent by 3 mm., 4.5 per cent by 4 mm., .5 per cent by 5 mm., 1 per cent by 6 mm., and .5 per cent by 7 mm. On the average, successive measurements varied by 1.43 mm., somewhat less than one per cent of the adult vole's total length. Occasional errors of two to four per cent were easily eliminated because for the voles used for growth records, series of measurements were available, with clearly defined trends. The occasional readings that deviated from the general trend for the individual were discarded.

Measurements were recorded along with other data in the field at the point of capture. Obtaining a reasonably accurate measurement on a live and struggling vole required patience and practice. With the thumb and forefinger of the left hand, I grasped the vole by loose skin of the nape, and simultaneously grasped the tail at a point approximately three-fourths of the distance to the tip. Then, with gentle but steady pressure, I stretched the vole out to its full length, meanwhile manipulating a millimeter ruler with the free fingers, so that the vole was pressed against it, with the nose pad at the end of the ruler.

The total length measurement is considered the best index to over-all size. The relative tail-length varies slightly between individuals, averaging approximately 22 per cent of the total length. Individuals having broken tails, or having the distal parts of their tails missing, were not included. The total length can be measured with greater accuracy than can either the head-and-body length or the tail-length separately.

GENERAL SOCIAL BEHAVIOR

As compared with other mammals, voles are tolerant and somewhat social. That individuals are not mutually exclusive (territorially) in areas occupied was demonstrated on many occasions when more than one individual was caught simultaneously in the same live-trap.

Injury of a vole by a trap-mate was a rare occurrence.

Multiple captures often involved a female in oestrus and one or more males, or a female and her young, but other instances involved various combinations of s.e.x and age groups. As many as five adults have been caught in a trap simultaneously at times when the population density was high. At such times, the meadow habitat is crossed by a maze of interconnecting surface runways and one runway may be traced continuously for 100 yards or more. Because each individual vole normally confines its activity to a small area, only a fraction of an acre, it is evident that individuals living at different places overlap in their home ranges, and also in the trailways followed in foraging. A high degree of tolerance is indicated. Where population is so spa.r.s.e that the systems of surface runways comprise separate and isolated units, trapping experience has shown that one such system may harbor several or many individuals.

As direct observations on voles under natural conditions are rarely feasible, because of the animals' timidity, their utilization of concealing cover, and tendency to crepuscular habits, best evidence of social habits and underground life is based upon behavior of captive individuals. Many voles were kept in confinement for varying lengths of times, either singly or in a.s.sociation with others. Under such conditions there was sometimes sporadic fighting, but it was mainly defensive and serious injuries were rare. Two or more voles caught at a given spot regardless of whether they were found in the same trap simultaneously, or trapped separately within a short time, usually were completely tolerant of each other. When at rest in their container, such voles would huddle together in a corner or in a nest, if materials were provided, so that collectively they presented the minimum exposed surface. The intimacy and lack of antagonism displayed on such occasions, suggested that the voles were accustomed to living together amicably in the same nest chamber. In live-trapping, "double" captures in a single trap often involved the same two individuals. Such trap-mates were often male and female, and in many instances the female was not in breeding condition. That the voles are not monogamous in habits was demonstrated when the same female was often trapped in a.s.sociation with either of two males. Other trap a.s.sociates taken together repeatedly often were two males, or two females. Voles that are nest mates or "neighbors" may tend to move about together in their foraging, or one confined in a trap may attract the other sufficiently to cause it to force an entrance by lifting the heavy door of a trap.

When a new vole, caught at a different location, is added to a container in which one or more are already confined, there is mutual circ.u.mspection between the original occupants and the newcomer. At first, each vole is intimidated by movements of the other, and as a result, the original occupants huddle in their established corner while the newcomer cowers in the most remote part of the container.

Gradually the voles become less timid and one may approach another slowly and cautiously, to sniff at it. The vole approached may react with a show of hostility which is largely defensive. In the characteristic posture of threat for defense, the vole crouches, or rears back on its haunches, with snout elevated and incisors prominently displayed. If the warning posture is unheeded, or if the vole is made unusually aggressive by having young to defend, or for some other reason, it attacks with a sudden forward lunge, striking the adversary simultaneously with both forefeet and with the incisors. The lunge is so rapid that when I have observed it, I have been unable to discern whether the attacker bit its opponent. The attack serves to force back the other animal, throwing it off balance and intimidating it. The attacked animal may dodge nimbly to avoid the lunge, but whether or not it is actually struck, it usually retreats, avoiding or postponing further hostilities. Voles that have been kept in containers for periods of hours or days tend to be more hostile and aggressive toward a newcomer than are those newly introduced. After series of meetings resulting from the exploratory behavior of the newcomer and the curiosity or normal activity of those longer confined, hostility gradually subsides.

Within a few hours a newcomer is usually accepted, and thenceforth he huddles with other members of the group when at rest, and hostility is rarely evident.

This ready acceptance on short acquaintance of strange voles into the family or social group suggests that lack of territoriality extends even to the use of the nest burrows, and that groups of voles may share the same nest, huddling together and deriving mutual benefit from the a.s.sociation, such as warmth in cold weather.

Schmidt (1931: 113), studying this vole in Clark County, Wisconsin, noted its colonial habits. He found isolated small mounds that were riddled with burrows, and little sign in intervening areas. At one mound he trapped two adult males, one adult female, and two young; at another mound, two adult males, two adult females, and four young were trapped. My individuals that were released from live-traps were on many occasions trailed by means of a stiff wire collar with spool of thread attached, to holes that presumably were their home burrows. Data obtained in this manner indicated that ordinarily several or many individuals use the same burrow system. The histories of individual voles on the study area at the Reservation indicate shift of home base from time to time, usually for short distances within the area already included in the home range, but occasionally to new areas relatively remote from the original home range.

Severe fighting between adult prairie voles occurs at times.

Occasionally, sharp squeaks accompanied by brisk rustling in the gra.s.s suggesting pursuit or conflict, are heard in their habitat. An unusually large adult male, long resident on a study area, suddenly lost weight and deteriorated in condition over a period of several days, then was found dead in a nest-box attached to a trap.

Dissection revealed numerous punctures in the skin and flesh of the neck and back, probably made by the incisors of another vole.

Extensive hemorrhage and swelling had occurred, and obviously these injuries were the cause of death.

Although it was not feasible to study the home life of the voles underground, clues were gained from those uncovered in runways and nests beneath large boards and strips of tarpaper, previously distributed for this purpose. Nests were constructed by the voles beneath several such pieces of tarpaper and runways appeared beneath all the pieces that were placed in habitat favorable to the voles.

In summer, however, the high daytime temperatures beneath these shelters made them uninhabitable to the voles, and they were used mainly in spring. From February 15 to May 1, 1953, 14 voles were caught 19 times beneath five of the tarpaper strips, and many other voles that were seen beneath them escaped. Upon turning one of the strips I often discovered voles in close proximity. Sometimes two or more darted from the same nest. The disturbance of repeatedly raising the strips and exposing the voles' shelters soon caused them to desert the sites; consequently the information obtained by this means was limited.

s.e.xUAL BEHAVIOR

There is s.e.xual activity in every month of the year, but its incidence varies greatly from one season to another. As has been indicated by various authors, male voles reach s.e.xual maturity later than females. It seems that ordinarily the availability of s.e.xually active males is not a limiting factor, however. While males that are still well below average adult size produce mature spermatozoa, and are probably capable of breeding (Jameson, 1947: 145), certain large old males may sire a disproportionately large percentage of the litters produced. Observations on males in confinement indicated that s.e.xual activity tended to be directly proportional to the size of the testes. Occasional individuals, having much enlarged scrotal testes were more readily stimulated to s.e.xual activity and more aggressive toward females than were those in which the testes were of more nearly typical size or abdominal or were smaller than normal. The combination of factors controlling size of testes is not well understood, but males having unusually large testes were caught most often when food supply was optimum, for instance after a period of heavy precipitation when an abundant supply of new gra.s.s provided succulent and nutritious food.

In confinement s.e.xual activity was largely inhibited and attempts to establish a laboratory colony met with failure. s.e.xual activity was observed mainly in recently captured males, and their interest was aroused chiefly by females that had given birth to litters within a few hours previously. Oestrus is known to follow closely after parturition. Females found in live-traps with newborn young often were brought to the laboratory for observation. An apparent instance of hostility between rival males competing for an oestrus female was observed on September 2, 1950. The female was found in a trap with four newborn young, and since the young had not yet attached to her teats, she was temporarily returned to the trap after recording, to prevent desertion of the litter. Returning twenty minutes later I found another adult vole at this trap. It would suddenly emerge from dense gra.s.s nearby, and would move over the trap or around it, with jerky, halting movements, then would dart back under cover. The female emerged from the nest box into the trap runway, and sniffed at the other, and both pressed against the intervening wire barrier.

There was gnawing on the wire by one or both. A third adult vole appeared. As it moved toward the trap, all three suddenly took alarm and darted back under cover, the female hiding in the trap nest box.

In a few seconds they again appeared. The two outsiders, presumably both males, were not individually recognizable, but several times one was seen to dart at the other, chasing it away momentarily. They were seldom both in sight at once.

Males confined with post-partum females usually evinced s.e.xual interest, following them about persistently and nuzzling their genitalia. The females, however, were often unreceptive perhaps because they were disturbed by strange surroundings and by the presence of their litters, so that they usually attempted to escape, or to rebuff the male's attention. At first the female might flee, squeaking in protest at the male's pursuit. If he still continued to follow, she would turn on him, rearing back in the characteristic threatening pose, and would lunge at him, striking him sharply or driving him back. After such rebuff, males were usually intimidated or discouraged so that they temporarily or permanently abandoned their advances, and small males were more easily rebuffed than were larger individuals. On several occasions large males having enlarged testes were not readily rebuffed by females but continued to follow them. When the female turned upon him, such a male might lunge against her, throwing her off balance, and causing her to attempt to escape, and then continuing the pursuit until it ended in copulation or in more severe fighting. Although not accepted s.e.xually, a rebuffed male might be readily accepted as a nest-mate, huddling along with the female and perhaps other individuals of both s.e.xes.

In huddling voles, the most frequently observed type of social behavior was grooming; one individual would slide its chin or muzzle through the other's fur with a stroking movement consisting of a series of rapid forward jerks and the stroking movements might continue for periods of minutes. The recipient of the grooming usually made no evident response indicative of either pleasure or displeasure. Often it seemed to be sleeping while the grooming was performed. Individuals of both s.e.xes performed this grooming and the recipient might be of either the same s.e.x or the opposite s.e.x. This grooming may have some significance as a search for ectoparasites such as fleas, or mites that often infest the voles. However, after prolonged grooming by a companion, a vole's fur was of mussed and disarranged appearance. Although the grooming that occurs between voles that are resting in nests seems to have no direct significance as s.e.xual behavior, somewhat similar actions const.i.tute part of the mating pattern. A s.e.xually aroused male overtaking a receptive female, slides his chin forward along her back with jerky, stroking movements. In some observed instances this behavior continued intermittently for several minutes before actual copulation. In some other instances it was almost lacking.

CHANGES IN FEMALE GENITALIA

In female voles that are s.e.xually quiescent, both those that have not yet attained breeding maturity, and those that have undergone regression after attainment of s.e.xual maturity, the v.a.g.i.n.al orifice is not evident. The ca.n.a.l is sealed externally by a membranous layer of epithelium. Presence of a v.a.g.i.n.al orifice indicates that the individual is in some active stage of the breeding cycle. The appearance of the orifice varies between different females, and it changes in the same female from day to day or even from hour to hour. Presumably these changes in the v.a.g.i.n.al orifice are cyclical and are closely correlated with oestrus, but attempts to trace them were unsuccessful largely because the normal cycle was rapidly suppressed in captive voles, which soon became s.e.xually quiescent.

Individual voles living under natural conditions were not trapped with sufficient regularity to permit tracing the details of changes in their genitalia.

In those females having the v.a.g.i.n.al orifice most developed, the margins are turgid and slightly inflamed. The circular opening gapes 1.0 to 1.5 mm. in diameter when the tail is raised. A female may remain in this condition for two days or more. v.a.g.i.n.al smears at this stage often showed nucleated cells characteristic of oestrus.

Subsequently the margins of the orifice become less prominent and the opening becomes smaller. The dorsal and ventral walls adhere until an opening is no longer evident unless the adjacent skin is stretched.

In pregnancy the orifice is occasionally sealed, but usually is evident. It is, however, less prominent than in oestrus, and does not gape. The margins are less turgid than in oestrus, and the opening is in the form of a transverse slit through which the purplish epithelial lining of the dorsal wall of the v.a.g.i.n.a can be seen. After parturition, placentae and b.l.o.o.d.y discharge often are in evidence in the v.a.g.i.n.al ca.n.a.l. Females that have not given birth to young recently may also have b.l.o.o.d.y mucous discharge. Its significance has not been determined. In females that are undergoing s.e.xual regression, the margins of the v.a.g.i.n.al orifice become shrunken and pale, and the orifice becomes partly or wholly sealed.

Bodenheimer and Sulman (1946:255) concluded from their study of _Microtus guentheri_ that in this species, as in "the cat," "the rabbit," "the ferret," and a few other mammals, ovulation is induced by copulation, and that there is no regular v.a.g.i.n.al cycle. Hoyte (1955:412) disagreed with these conclusions for other species of _Microtus_, as he trapped individuals of _M. oeconomus_ that had recently ovulated without copulation (at least no sperm were found in the genital tracts). In _M. ochrogaster_ oestrus seems to be controlled largely by the food supply, at least the incidence of perforate females was found to fluctuate irregularly tending to follow the trend of rainfall, and, probably in more direct correlation, the amount of new gra.s.s present (see Table 1, and Martin, 1956:383-384). It therefore seems unlikely that in this species ovulation is dependent on copulation.

In females that have not yet produced young the teats are minute and well concealed in the fur, so that they are difficult to find, but in lactation they become conspicuous. In early lactation the teats are typically about 1 mm. in diameter and 2.5 mm. in length. As lactation progresses, they become thickened to nearly twice the original diameter. After lactation, as inversion occurs, they shrink to scabrous low prominences, 2 mm. to 3 mm. in diameter, surrounded by bare skin. There are three pairs of mammae, one pair pectoral and the other two abdominal. As mentioned by Jameson (1947:146), the pectoral mammae show little evidence of use in lactating prairie voles. Probably they are not used at all except in females with more than the four young in a litter accommodated by the abdominal mammae. As in various other rodents, the suckling young may cling to the female's teats and may be dragged over the ground as she moves about. When the female forages near the nest, she may drag the young with her instead of leaving them, but she can detach them instantly if she so desires. On many occasions females found in live-traps had young that were several days old clinging to their teats. In some instances young that had their eyes open may have followed the female into the trap and attached afterward.

SEASONAL INCIDENCE OF BREEDING

In the region of my study the prairie vole breeds the year round, but the rate of breeding changes continually. There is no regularity in the trend of the breeding season from year to year. It is obvious that the species is responsive to environmental changes and is so well attuned that its breeding is speedily initiated or inhibited by changes to favorable or unfavorable weather. The incidence of breeding is highest when temperature is moderate and both water and foods of preferred sorts are plentiful.

Tables 1 and 2 and Fig. 1, based on 11,109 records representing each month over a four-year period, show the changing trends from month to month. The perforate condition recorded in Table 1 may represent any of several stages in oestrus or pregnancy, but is regarded as a crude index of rate of breeding, since voles in the anoestrus stage lack the v.a.g.i.n.al orifice. Highest percentages of perforate females occurred in the months of February, March, April, May, and June, while by far the lowest percentages were recorded in the drought summers of 1952 and 1953. Even in mid-winter a substantial proportion of the females trapped were perforate.

[Ill.u.s.tration: FIG. 1. Average catch per day in a three-acre field, in a grid of 100 live-traps, over a four-year period. For each year, solid line represents total and dashed line represents number of young up to 30 grams in weight. Numbers caught are roughly indicative of population density, but many variables distort this relationship. Young are never represented in the catch in their true ratio to adults, since on the average they are less vagile and less attracted to traps.]

Table 1. Percentages of Adult Females Recorded as Perforate in the Monthly Samples From 1950 Through 1953.